WHIRLY1 Regulates HSP21.5A Expression to Promote Thermotolerance in Tomato

Abstract

Heat stress poses a major threat to plant productivity and crop yields. The induction of heat shock proteins (HSPs) by heat shock factors is a principal defense response of plants exposed to heat stress. In this study, we identified and analyzed the heat stress-induced Whirly1 (SlWHY1) gene in tomato (Solanum lycopersicum). We generated various SlWHY1-overexpressing (OE) and SlWHY1-RNA interference (RNAi) lines to investigate the role of WHIRLY1 in thermotolerance. Compared with the wild type (WT), the OE lines showed less wilting, as reflected by their increased membrane stability and soluble sugar content and reduced reactive oxygen species (ROS) accumulation under heat stress. By contrast, RNAi lines with inhibited SlWHY1 expression showed the opposite phenotype and corresponding physiological indices under heat stress. The heat-induced gene SlHSP21.5A, encoding an endoplasmic reticulum-localized HSP, was upregulated in the OE lines and downregulated in the RNAi lines compared with the WT. RNAi-mediated inhibition of SlHSP21.5A expression also resulted in reduced membrane stability and soluble sugar content and increased ROS accumulation under heat stress compared with the WT. SlWHY1 binds to the elicitor response element-like element in the promoter of SlHSP21.5A to activate its transcription. These findings suggest that SlWHY1 promotes thermotolerance in tomato by regulating SlHSP21.5A expression.

WHIRLIES Are Multifunctional DNA-Binding Proteins With Impact on Plant Development and Stress Resistance

“…In tomato, overexpression of WHIRLY1 leads to higher chilling tolerance, coinciding with a higher level of soluble sugars and higher photosynthesis likely due to enhanced expression of RBCS1 ( Zhuang et al, 2020b ) as well as to enhanced thermotolerance ( Zhuang et al, 2020a ). Taken together, these results indicate that the WHIRLY proteins have a positive impact on abiotic stress resistance in dicot plants.…”

Roles of brassinosteroids in plant growth and abiotic stress response

“…High-temperature stress can also cause severe damage to physiological metabolism and growth and development of plants (Zhuang et al 2020;Sun et al 2019a;Wang et al 2010Wang et al , 2015bWang et al , 2019a. Heat damage to plants includes direct damage and indirect damage.…”

WHIRLY1 recruits the histone deacetylase HDA15 repressing leaf senescence and flowering in Arabidopsis

“…In chloroplasts, WHY1 is involved in maintaining chloroplast genome stability with specific roles in DNA replication and organelle DNA repair, as well as RNA processing (Prikryl et al, 2008;Etminan et al, 2010;Cappadocia et al, 2012;Krupinska et al, 2014b;Wang et al, 2021). WHY1 also affects reactive oxygen species redox signaling in photosystem I (Huang et al, 2017;Zhuang et al, 2018Zhuang et al, , 2020. In the nucleus, WHY1 acts as a transcriptional activator, binding to the inverted repeat sequence of the elicitor response element (ERE) in the promoter region of pathogenesis-related gene PR-10a to participate in salicylic acid-dependent plant disease resistance response, binding an ERE-like element of SlHSP21.5A to promote thermotolerance in tomato (Zhuang et al, 2020).…”

“…WHY1 also affects reactive oxygen species redox signaling in photosystem I (Huang et al, 2017;Zhuang et al, 2018Zhuang et al, , 2020. In the nucleus, WHY1 acts as a transcriptional activator, binding to the inverted repeat sequence of the elicitor response element (ERE) in the promoter region of pathogenesis-related gene PR-10a to participate in salicylic acid-dependent plant disease resistance response, binding an ERE-like element of SlHSP21.5A to promote thermotolerance in tomato (Zhuang et al, 2020). In addition, WHY1 plays important roles in leaf senescence by regulating senescence marker genes HvS40 and AtWRKY53 (Hinderhofer and Zentgraf, 2001;Miao et al, 2013;Krupinska et al, 2014a).…”